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Bioinductive Scaffolds—Powerhouses of Skeletal Muscle Tissue Engineering

  • Wound Healing and Tissue Repair (CC Yates, Section Editor)
  • Published:
Current Pathobiology Reports

Abstract

Purpose of Review

Skeletal muscle tissue engineering is a field of vital importance to many sufferers of volumetric muscle loss (VML) and other muscular pathologies. Bioinductive scaffolds can host cells and modulate their behaviour and thus serve as a platform for muscle tissue growth.

Recent Findings

Scaffolds for skeletal muscle engineering can be composed of synthetic polymers, naturally derived polymers, decellularized extracellular matrix (ECM) or any combination of these. They lead to active tissue regeneration by modulating the initial inflammatory response, recruiting progenitor cells and determining cell phenotype. Their breakdown allows cellular migration while releasing stored stimulatory compounds.

Summary

Understanding the effects and advantages of the different biomaterial options might facilitate the design of novel scaffolds that support muscular regeneration, thereby restoring function and appearance to ailing patients. This review aims to present the latest advances in scaffold-based skeletal muscle tissue regeneration.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Janssen I, Heymsfield SB, Wang ZM, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. Journal of applied physiology (Bethesda, Md: 1985). 2000;89(1):81–8.

    CAS  Google Scholar 

  2. Jarvinen TA, Jarvinen TL, Kaariainen M, Kalimo H, Jarvinen M. Muscle injuries: biology and treatment. Am J Sports Med. 2005;33(5):745–64.

    Article  PubMed  Google Scholar 

  3. Almekinders LC, Gilbert JA. Healing of experimental muscle strains and the effects of nonsteroidal antiinflammatory medication. Am J Sports Med. 1986;14(4):303–8.

    Article  CAS  PubMed  Google Scholar 

  4. Ikemoto-Uezumi M, Uezumi A, Tsuchida K, Fukada S, Yamamoto H, Yamamoto N, et al. Pro-insulin-like growth factor-II ameliorates age-related inefficient regenerative response by orchestrating self-reinforcement mechanism of muscle regeneration. Stem cells (Dayton, Ohio). 2015;33(8):2456–68.

    Article  CAS  Google Scholar 

  5. Ye F, Mathur S, Liu M, Borst SE, Walter GA, Sweeney HL, et al. Overexpression of insulin-like growth factor-1 attenuates skeletal muscle damage and accelerates muscle regeneration and functional recovery after disuse. Exp Physiol. 2013;98(5):1038–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Takahashi T, Ishida K, Itoh K, Konishi Y, Yagyu KI, Tominaga A, et al. IGF-I gene transfer by electroporation promotes regeneration in a muscle injury model. Gene Ther. 2003;10(8):612–20.

    Article  CAS  PubMed  Google Scholar 

  7. Armand AS, Launay T, Pariset C, Della Gaspera B, Charbonnier F, Chanoine C. Injection of FGF6 accelerates regeneration of the soleus muscle in adult mice. Biochim Biophys Acta. 2003;1642(1–2):97–105.

    Article  CAS  PubMed  Google Scholar 

  8. Hwang JH, Kim IG, Piao S, Jung AR, Lee JY, Park KD, et al. Combination therapy of human adipose-derived stem cells and basic fibroblast growth factor hydrogel in muscle regeneration. Biomaterials. 2013;34(25):6037–45.

    Article  CAS  PubMed  Google Scholar 

  9. Kelc R, Trapecar M, Gradisnik L, Rupnik MS, Vogrin M. Platelet-rich plasma, especially when combined with a TGF-beta inhibitor promotes proliferation, viability and myogenic differentiation of myoblasts in vitro. PLoS One. 2015;10(2):e0117302.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Chan YS, Li Y, Foster W, Fu FH, Huard J. The use of suramin, an antifibrotic agent, to improve muscle recovery after strain injury. Am J Sports Med. 2005;33(1):43–51.

    Article  PubMed  Google Scholar 

  11. Fukushima K, Badlani N, Usas A, Riano F, Fu F, Huard J. The use of an antifibrosis agent to improve muscle recovery after laceration. Am J Sports Med. 2001;29(4):394–402.

    Article  CAS  PubMed  Google Scholar 

  12. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A, et al. Direct isolation of satellite cells for skeletal muscle regeneration. Science (New York, NY). 2005;309(5743):2064–7.

    Article  CAS  Google Scholar 

  13. van Wachem PB, Brouwer LA, van Luyn MJ. Absence of muscle regeneration after implantation of a collagen matrix seeded with myoblasts. Biomaterials. 1999;20(5):419–26.

    Article  PubMed  Google Scholar 

  14. Borselli C, Cezar CA, Shvartsman D, Vandenburgh HH, Mooney DJ. The role of multifunctional delivery scaffold in the ability of cultured myoblasts to promote muscle regeneration. Biomaterials. 2011;32(34):8905–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Borschel GH, Dow DE, Dennis RG, Brown DL. Tissue-engineered axially vascularized contractile skeletal muscle. Plast Reconstr Surg. 2006;117(7):2235–42.

    Article  CAS  PubMed  Google Scholar 

  16. Corona BT, Machingal MA, Criswell T, Vadhavkar M, Dannahower AC, Bergman C, et al. Further development of a tissue engineered muscle repair construct in vitro for enhanced functional recovery following implantation in vivo in a murine model of volumetric muscle loss injury. Tissue Eng A. 2012;18(11–12):1213–28.

    Article  CAS  Google Scholar 

  17. Machingal MA, Corona BT, Walters TJ, Kesireddy V, Koval CN, Dannahower A, et al. A tissue-engineered muscle repair construct for functional restoration of an irrecoverable muscle injury in a murine model. Tissue Eng A. 2011;17(17–18):2291–303.

    Article  CAS  Google Scholar 

  18. Skuk D. Acute rejection of myofibers in nonhuman primates: key histopathologic features. J Neuropathol Exp Neurol. 2012;71(5):398–412.

    Article  PubMed  Google Scholar 

  19. Conconi MT, De Coppi P, Bellini S, Zara G, Sabatti M, Marzaro M, et al. Homologous muscle acellular matrix seeded with autologous myoblasts as a tissue-engineering approach to abdominal wall-defect repair. Biomaterials. 2005;26(15):2567–74.

    Article  CAS  PubMed  Google Scholar 

  20. Park S, Choi Y, Jung N, Yu Y, Ryu KH, Kim HS, et al. Myogenic differentiation potential of human tonsil-derived mesenchymal stem cells and their potential for use to promote skeletal muscle regeneration. Int J Mol Med. 2016;37(5):1209–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Fujita R, Tamai K, Aikawa E, Nimura K, Ishino S, Kikuchi Y, et al. Endogenous mesenchymal stromal cells in bone marrow are required to preserve muscle function in mdx mice. Stem cells (Dayton, Ohio). 2015;33(3):962–75.

    Article  CAS  Google Scholar 

  22. Nakamura Y, Miyaki S, Ishitobi H, Matsuyama S, Nakasa T, Kamei N, et al. Mesenchymal-stem-cell-derived exosomes accelerate skeletal muscle regeneration. FEBS Lett. 2015;589(11):1257–65.

    Article  CAS  PubMed  Google Scholar 

  23. Jeong J, Shin K, Lee SB, Lee DR, Kwon H. Patient-tailored application for Duchene muscular dystrophy on mdx mice based induced mesenchymal stem cells. Exp Mol Pathol. 2014;97(2):253–8.

    Article  CAS  PubMed  Google Scholar 

  24. von Roth P, Duda GN, Radojewski P, Preininger B, Perka C, Winkler T. Mesenchymal stem cell therapy following muscle trauma leads to improved muscular regeneration in both male and female rats. Gender medicine. 2012;9(2):129–36.

    Article  Google Scholar 

  25. Merritt EK, Cannon MV, Hammers DW, Le LN, Gokhale R, Sarathy A, et al. Repair of traumatic skeletal muscle injury with bone-marrow-derived mesenchymal stem cells seeded on extracellular matrix. Tissue Eng A. 2010;16(9):2871–81.

    Article  CAS  Google Scholar 

  26. Carnio S, Serena E, Rossi CA, De Coppi P, Elvassore N, Vitiello L. Three-dimensional porous scaffold allows long-term wild-type cell delivery in dystrophic muscle. J Tissue Eng Regen Med. 2011;5(1):1–10.

    Article  CAS  PubMed  Google Scholar 

  27. Oliva F, Via AG, Kiritsi O, Foti C, Maffulli N. Surgical repair of muscle laceration: biomechanical properties at 6 years follow-up. Muscles, ligaments and tendons journal. 2013;3(4):313–7.

    PubMed  Google Scholar 

  28. Kragh JF Jr, Svoboda SJ, Wenke JC, Ward JA, Walters TJ. Epimysium and perimysium in suturing in skeletal muscle lacerations. J Trauma. 2005;59(1):209–12.

    Article  PubMed  Google Scholar 

  29. Menetrey J, Kasemkijwattana C, Fu FH, Moreland MS, Huard J. Suturing versus immobilization of a muscle laceration. A morphological and functional study in a mouse model. Am J Sports Med. 1999;27(2):222–9.

    Article  CAS  PubMed  Google Scholar 

  30. Äärimaa V, Kääriäinen M, Vaittinen S, Tanner J, Järvinen T, Best T, et al. Restoration of myofiber continuity after transection injury in the rat soleus. Neuromuscul Disord. 2004;14(7):421–8.

    Article  PubMed  Google Scholar 

  31. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407(6801):249–57.

    Article  CAS  PubMed  Google Scholar 

  32. Turner NJ, Badylak SF. Regeneration of skeletal muscle. Cell Tissue Res. 2012;347(3):759–74.

    Article  PubMed  Google Scholar 

  33. Järvinen TA, Järvinen TL, Kääriäinen M, Kalimo H, Järvinen M. Muscle injuries biology and treatment. Am J Sports Med. 2005;33(5):745–64.

    Article  PubMed  Google Scholar 

  34. Hurme T, Kalimo H, Lehto M, Jarvinen M. Healing of skeletal muscle injury: an ultrastructural and immunohistochemical study. Med Sci Sports Exerc. 1991;23(7):801–10.

    Article  CAS  PubMed  Google Scholar 

  35. Brigitte M, Schilte C, Plonquet A, Baba-Amer Y, Henri A, Charlier C, et al. Muscle resident macrophages control the immune cell reaction in a mouse model of notexin-induced myoinjury. Arthritis Rheum. 2010;62(1):268–79.

    Article  CAS  PubMed  Google Scholar 

  36. Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, Plonquet A, et al. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med. 2007;204(5):1057–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Villalta SA, Nguyen HX, Deng B, Gotoh T, Tidball JG. Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum Mol Genet. 2009;18(3):482–96.

    Article  CAS  PubMed  Google Scholar 

  38. Badylak SF. Host response to biomaterials: the impact of host response on biomaterial selection. New York: Elsevier Science; 2015.

    Google Scholar 

  39. Molea G, Schonauer F, Bifulco G, D'Angelo D. Comparative study on biocompatibility and absorption times of three absorbable monofilament suture materials (Polydioxanone, Poliglecaprone 25, Glycomer 631). Br J Plast Surg. 2000;53(2):137–41.

    Article  CAS  PubMed  Google Scholar 

  40. Lam CX, Savalani MM, Teoh S-H, Hutmacher DW. Dynamics of in vitro polymer degradation of polycaprolactone-based scaffolds: accelerated versus simulated physiological conditions. Biomed Mater. 2008;3(3):034108.

    Article  PubMed  Google Scholar 

  41. Williamson MR, Adams EF, Coombes AGA. Gravity spun polycaprolactone fibres for soft tissue engineering: interaction with fibroblasts and myoblasts in cell culture. Biomaterials. 2006;27(7):1019–26.

    Article  CAS  PubMed  Google Scholar 

  42. McKeon-Fischer K, Flagg D, Freeman J. Coaxial electrospun poly (ε-caprolactone), multiwalled carbon nanotubes, and polyacrylic acid/polyvinyl alcohol scaffold for skeletal muscle tissue engineering. J Biomed Mater Res A. 2011;99(3):493–9.

    Article  CAS  PubMed  Google Scholar 

  43. Bian W, Bursac N. Tissue engineering of functional skeletal muscle: challenges and recent advances. IEEE engineering in medicine and biology magazine: the quarterly magazine of the Engineering in Medicine & Biology Society. 2008;27(5):109–13.

    Article  Google Scholar 

  44. • Zhao W, Ju YM, Christ G, Atala A, Yoo JJ, Lee SJ. Diaphragmatic muscle reconstruction with an aligned electrospun poly(ε-caprolactone)/collagen hybrid scaffold. Biomaterials. 2013;34(33):8235–40. This study showed positive scaffold-mediated muscle regeneration in a model with clear clinical translatability. It provided a good example of a composite natural/synthetic polymer.

    Article  CAS  PubMed  Google Scholar 

  45. Zambon JP, de Sa Barretto LS, Nakamura AN, Duailibi S, Leite K, Magalhaes RS, et al. Histological changes induced by Polyglycolic-Acid (PGA) scaffolds seeded with autologous adipose or muscle-derived stem cells when implanted on rabbit bladder. Organ. 2014;10(2):278–88.

    Google Scholar 

  46. Harris LD, Kim BS, Mooney DJ. Open pore biodegradable matrices formed with gas foaming. J Biomed Mater Res. 1998;42(3):396–402.

    Article  CAS  PubMed  Google Scholar 

  47. Peters MC, Polverini PJ, Mooney DJ. Engineering vascular networks in porous polymer matrices. J Biomed Mater Res. 2002;60(4):668–78.

    Article  CAS  PubMed  Google Scholar 

  48. Yang HS, Ieronimakis N, Tsui JH, Kim HN, Suh K-Y, Reyes M, et al. Nanopatterned muscle cell patches for enhanced myogenesis and dystrophin expression in a mouse model of muscular dystrophy. Biomaterials. 2014;35(5):1478–86.

    Article  CAS  PubMed  Google Scholar 

  49. Wang P-Y, Wu T-H, Tsai W-B, Kuo W-H, Wang M-J. Grooved PLGA films incorporated with RGD/YIGSR peptides for potential application on skeletal muscle tissue engineering. Colloids Surf B: Biointerfaces. 2013;110:88–95.

    Article  CAS  PubMed  Google Scholar 

  50. Thorrez L, Shansky J, Wang L, Fast L, VandenDriessche T, Chuah M, et al. Growth, differentiation, transplantation and survival of human skeletal myofibers on biodegradable scaffolds. Biomaterials. 2008;29(1):75–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. • Manchineella S, Thrivikraman G, Khanum KK, Ramamurthy PC, Basu B, Govindaraju T. Pigmented silk nanofibrous composite for skeletal muscle tissue engineering. Advanced healthcare materials. 2016;5(10):1222–32. The authors concentrated on the electroactive properties of MPCs when developing the scaffold described in this study. They characterized its electrical properties and demonstrated its in vitro myogenic capabilities.

    Article  CAS  PubMed  Google Scholar 

  52. •• Shin YC, Lee JH, Jin L, Kim MJ, Kim YJ, Hyun JK, et al. Stimulated myoblast differentiation on graphene oxide-impregnated PLGA-collagen hybrid fibre matrices. Journal of nanobiotechnology. 2015;13:21. This study is an impressive example of an advanced biomaterial, formed from a composite of PLGA with collagen and graphene, with potential for skeletal muscle tissue engineering.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Mayer U. Integrins: redundant or important players in skeletal muscle? J Biol Chem. 2003;278(17):14587–90.

    Article  CAS  PubMed  Google Scholar 

  54. Chiron S, Tomczak C, Duperray A, Laine J, Bonne G, Eder A, et al. Complex interactions between human myoblasts and the surrounding 3D fibrin-based matrix. PLoS One. 2012;7(4):e36173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Rybalko VY, Pham CB, Hsieh PL, Hammers DW, Merscham-Banda M, Suggs LJ, et al. Controlled delivery of SDF-1alpha and IGF-1: CXCR4(+) cell recruitment and functional skeletal muscle recovery. Biomaterials science. 2015;3(11):1475–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Di Lullo GA, Sweeney SM, Korkko J, Ala-Kokko L, San Antonio JD. Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, type I collagen. J Biol Chem. 2002;277(6):4223–31.

    Article  PubMed  Google Scholar 

  57. Kroehne V, Heschel I, Schugner F, Lasrich D, Bartsch JW, Jockusch H. Use of a novel collagen matrix with oriented pore structure for muscle cell differentiation in cell culture and in grafts. J Cell Mol Med. 2008;12(5a):1640–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Dai W, Hale SL, Kay GL, Jyrala AJ, Kloner RA. Delivering stem cells to the heart in a collagen matrix reduces relocation of cells to other organs as assessed by nanoparticle technology. Regen Med. 2009;4(3):387–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Smith AS, Passey SL, Martin NR, Player DJ, Mudera V, Greensmith L, et al. Creating interactions between tissue-engineered skeletal muscle and the peripheral nervous system. Cells Tissues Organs. 2016;202(3–4):143–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Boyd A, Chakrabarty AM. Pseudomonas aeruginosa biofilms: role of the alginate exopolysaccharide. J Ind Microbiol. 1995;15(3):162–8.

    Article  CAS  PubMed  Google Scholar 

  61. Rowley JA, Madlambayan G, Mooney DJ. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials. 1999;20(1):45–53.

    Article  CAS  PubMed  Google Scholar 

  62. Stilhano RS, Madrigal JL, Wong K, Williams PA, Martin PK, Yamaguchi FS, et al. Injectable alginate hydrogel for enhanced spatiotemporal control of lentivector delivery in murine skeletal muscle. Journal of controlled release : official journal of the Controlled Release Society. 2016;237:42–9.

    Article  CAS  Google Scholar 

  63. Raya B, Caroline C, Daniel C, Benjamin D, Christophe T, Philippe B, et al. Elaboration and evaluation of alginate foam scaffolds for soft tissue engineering. Int J Pharm. 2017;524(1):433–42.

  64. Hill E, Boontheekul T, Mooney DJ. Designing scaffolds to enhance transplanted myoblast survival and migration. Tissue Eng. 2006;12(5):1295–304.

    Article  CAS  PubMed  Google Scholar 

  65. Pumberger M, Qazi TH, Ehrentraut MC, Textor M, Kueper J, Stoltenburg-Didinger G, et al. Synthetic niche to modulate regenerative potential of MSCs and enhance skeletal muscle regeneration. Biomaterials. 2016;99:95–108.

    Article  CAS  PubMed  Google Scholar 

  66. Stilhano RS, Madrigal JL, Wong K, Williams PA, Martin PKM, Yamaguchi FSM, et al. Injectable alginate hydrogel for enhanced spatiotemporal control of lentivector delivery in murine skeletal muscle. J Control Release. 2016;237:42–9.

    Article  CAS  PubMed  Google Scholar 

  67. Wang W, Fan M, Zhang L, Liu SH, Sun L, Wang CY. Compatibility of hyaluronic acid hydrogel and skeletal muscle myoblasts. Biomedical materials (Bristol, England). 2009;4(2):025011.

    Article  Google Scholar 

  68. Rossi CA, Flaibani M, Blaauw B, Pozzobon M, Figallo E, Reggiani C, et al. In vivo tissue engineering of functional skeletal muscle by freshly isolated satellite cells embedded in a photopolymerizable hydrogel. FASEB J. 2011;25(7):2296–304.

    Article  CAS  PubMed  Google Scholar 

  69. Desiderio V, De Francesco F, Schiraldi C, De Rosa A, La Gatta A, Paino F, et al. Human Ng2+ adipose stem cells loaded in vivo on a new crosslinked hyaluronic acid-lys scaffold fabricate a skeletal muscle tissue. J Cell Physiol. 2013;228(8):1762–73.

    Article  CAS  PubMed  Google Scholar 

  70. Kong WH, Sung DK, Kim H, Yang J-A, Ieronimakis N, Kim KS, et al. Self-adjuvanted hyaluronate—antigenic peptide conjugate for transdermal treatment of muscular dystrophy. Biomaterials. 2016;81:93–103.

    Article  CAS  PubMed  Google Scholar 

  71. Rosso F, Giordano A, Barbarisi M, Barbarisi A. From cell–ECM interactions to tissue engineering. J Cell Physiol. 2004;199(2):174–80.

    Article  CAS  PubMed  Google Scholar 

  72. Keane TJ, Swinehart IT, Badylak SF. Methods of tissue decellularization used for preparation of biologic scaffolds and in vivo relevance. Methods (San Diego, Calif). 2015;84:25–34.

    Article  CAS  Google Scholar 

  73. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126(4):677–89.

    Article  CAS  PubMed  Google Scholar 

  74. Engler AJ, Griffin MA, Sen S, Bönnemann CG, Sweeney HL, Discher DE. Myotubes differentiate optimally on substrates with tissue-like stiffness. J Cell Biol. 2004;166(6):877–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Casar JC, Cabello-Verrugio C, Olguin H, Aldunate R, Inestrosa NC, Brandan E. Heparan sulfate proteoglycans are increased during skeletal muscle regeneration: requirement of syndecan-3 for successful fiber formation. J Cell Sci. 2004;117(1):73–84.

    Article  CAS  PubMed  Google Scholar 

  76. Casar JC, McKechnie BA, Fallon JR, Young MF, Brandan E. Transient up-regulation of biglycan during skeletal muscle regeneration: delayed fiber growth along with decorin increase in biglycan-deficient mice. Dev Biol. 2004;268(2):358–71.

    Article  CAS  PubMed  Google Scholar 

  77. El Fahime E, Torrente Y, Caron NJ, Bresolin MD, Tremblay JP. In vivo migration of transplanted myoblasts requires matrix metalloproteinase activity. Exp Cell Res. 2000;258(2):279–87.

    Article  PubMed  Google Scholar 

  78. Lewis M, Tippett H, Sinanan A, Morgan M, Hunt N. Gelatinase-B (matrix metalloproteinase-9; MMP-9) secretion is involved in the migratory phase of human and murine muscle cell cultures. Journal of Muscle Research & Cell Motility. 2000;21(3):223–33.

    Article  CAS  Google Scholar 

  79. Rifkin DB, Mazzieri R, Munger JS, Noguera I, Sung J. Proteolytic control of growth factor availability. APMIS. 1999;107(1–6):80–5.

    Article  CAS  PubMed  Google Scholar 

  80. Brennan EP, Tang X-H, Stewart-Akers AM, Gudas LJ, Badylak SF. Chemoattractant activity of degradation products of fetal and adult skin extracellular matrix for keratinocyte progenitor cells. J Tissue Eng Regen Med. 2008;2(8):491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Agrawal V, Kelly J, Tottey S, Daly KA, Johnson SA, Siu BF, et al. An isolated cryptic peptide influences osteogenesis and bone remodeling in an adult mammalian model of digit amputation. Tissue Engineering - Part A. 2011;17(23–24):3033–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Tottey S, Corselli M, Jeffries EM, Londono R, Peault B, Badylak SF. Extracellular matrix degradation products and low-oxygen conditions enhance the regenerative potential of perivascular stem cells. Tissue Eng A. 2010;17(1–2):37–44.

    Google Scholar 

  83. Matrisian LM. Metalloproteinases and their inhibitors in matrix remodeling. Trends Genet. 1990;6:121–5.

    Article  CAS  PubMed  Google Scholar 

  84. Mannello F, Tonti GA, Bagnara GP, Papa S. Role and function of matrix metalloproteinases in the differentiation and biological characterization of mesenchymal stem cells. Stem cells (Dayton, Ohio). 2006;24(3):475–81.

    Article  CAS  Google Scholar 

  85. Porzionato A, Sfriso MM, Pontini A, Macchi V, Petrelli L, Pavan PG, et al. Decellularized human skeletal muscle as biologic scaffold for reconstructive surgery. Int J Mol Sci. 2015;16(7):14808–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Wilson K, Terlouw A, Roberts K, Wolchok JC. The characterization of decellularized human skeletal muscle as a blueprint for mimetic scaffolds. Journal of materials science Materials in medicine. 2016;27(8):125.

    Article  PubMed  Google Scholar 

  87. Sicari BM, Agrawal V, Siu BF, Medberry CJ, Dearth CL, Turner NJ, et al. A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng A. 2012;18(19–20):1941–8.

    Article  CAS  Google Scholar 

  88. Chen XK, Walters TJ. Muscle-derived decellularised extracellular matrix improves functional recovery in a rat latissimus dorsi muscle defect model. Journal of plastic, reconstructive & aesthetic surgery : JPRAS. 2013;66(12):1750–8.

    Article  Google Scholar 

  89. Stern MM, Myers RL, Hammam N, Stern KA, Eberli D, Kritchevsky SB, et al. The influence of extracellular matrix derived from skeletal muscle tissue on the proliferation and differentiation of myogenic progenitor cells ex vivo. Biomaterials. 2009;30(12):2393–9.

    Article  CAS  PubMed  Google Scholar 

  90. Turner NJ, Yates AJ Jr, Weber DJ, Qureshi IR, Stolz DB, Gilbert TW, et al. Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction. Tissue Eng A. 2010;16(11):3309–17.

    Article  CAS  Google Scholar 

  91. Valentin JE, Turner NJ, Gilbert TW, Badylak SF. Functional skeletal muscle formation with a biologic scaffold. Biomaterials. 2010;31(29):7475–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Valentin JE, Badylak JS, McCabe GP, Badylak SF. Extracellular matrix bioscaffolds for orthopaedic applications. A comparative histologic study. J Bone Joint Surg. 2006;88(12):2673–86.

    PubMed  Google Scholar 

  93. McClelland R, Wauthier E, Uronis J, Reid L. Gradients in the liver’s extracellular matrix chemistry from periportal to pericentral zones: influence on human hepatic progenitors. Tissue Eng A. 2008;14(1):59–70.

    Article  CAS  Google Scholar 

  94. Zhang Y, He Y, Bharadwaj S, Hammam N, Carnagey K, Myers R, et al. Tissue-specific extracellular matrix coatings for the promotion of cell proliferation and maintenance of cell phenotype. Biomaterials. 2009;30(23):4021–8.

    Article  CAS  PubMed  Google Scholar 

  95. Cheng NC, Estes BT, Awad HA, Guilak F. Chondrogenic differentiation of adipose-derived adult stem cells by a porous scaffold derived from native articular cartilage extracellular matrix. Tissue Eng A. 2009;15(2):231–41.

    Article  CAS  Google Scholar 

  96. • Keane TJ, DeWard A, Londono R, Saldin LT, Castleton AA, Carey L, et al. Tissue-specific effects of esophageal extracellular matrix. Tissue Eng A. 2015;21(17–18):2293–300. The authors of this study convincingly demonstrated the advantages of site-specific ECM for in vitro differentiation, maturation and proliferation of stem cells. Translation of these properties to an in vivo setting would be a big boost to the field.

    Article  CAS  Google Scholar 

  97. Wolf MT, Daly KA, Reing JE, Badylak SF. Biologic scaffold composed of skeletal muscle extracellular matrix. Biomaterials. 2012;33(10):2916–25.

    Article  CAS  PubMed  Google Scholar 

  98. Kasukonis B, Kim J, Brown L, Jones J, Ahmadi S, Washington T, et al. Codelivery of infusion decellularized skeletal muscle with minced muscle autografts improved recovery from volumetric muscle loss injury in a rat model. Tissue Eng A. 2016;22(19–20):1151–63.

    Article  CAS  Google Scholar 

  99. Corona BT, Garg K, Ward CL, McDaniel JS, Walters TJ, Rathbone CR. Autologous minced muscle grafts: a tissue engineering therapy for the volumetric loss of skeletal muscle. Am J Phys Cell Phys. 2013;305(7):C761–75.

    Article  CAS  Google Scholar 

  100. Knappe S, Zammit P, Knight R. A population of Pax7-expressing muscle progenitor cells show differential responses to muscle injury dependent on developmental stage and injury extent. Front Aging Neurosci. 2015;7:161.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Hsu M, Peled ZM, Chin GS, Liu W, Longaker MT. Ontogeny of expression of transforming growth factor-beta 1 (TGF-beta 1), TGF-beta 3, and TGF-beta receptors I and II in fetal rat fibroblasts and skin. Plast Reconstr Surg. 2001;107(7):1787–94. discussion 1795-6

    Article  CAS  PubMed  Google Scholar 

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  1. 300 E Superior Tarry Building, Suite 4-720, Chicago, IL, 60611, USA

    Hari Iyer

  2. Northwestern University Feinberg School of Medicine, Galter 19-250, 675 N. St. Clair Street, Chicago, IL, 60611, USA

    Robert D. Galiano

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  1. Hari Iyer
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This article is part of the Topical Collection on Wound Healing and Tissue Repair

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Iyer, H., Galiano, R.D. Bioinductive Scaffolds—Powerhouses of Skeletal Muscle Tissue Engineering. Curr Pathobiol Rep 5, 279–288 (2017). https://doi.org/10.1007/s40139-017-0151-9

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